Ring species as demonstrations of the continuum of species formation

Abstract

In the mid-20th century, Ernst Mayr (1942) and Theodosius Dobzhansky (1958) championed the significance of 'circular overlaps' or 'ring species' as the perfect demonstration of the gradual nature of species formation. As an ancestral species expands its range, wrapping around a geographic barrier, derived taxa within the ring display interactions typical of populations, such as genetic and morphological intergradation, while overlapping taxa at the terminus of the ring behave largely as sympatric, reproductively isolated species. Are ring species extremely rare or are they just difficult to detect? What conditions favour their formation? Modelling studies have attempted to address these knowledge gaps by estimating the biological parameters that result in stable ring species (Martins et al. 2013), and determining the necessary topographic parameters of the barriers encircled (Monahan et al. 2012). However, any generalization is undermined by a major limitation: only a handful of ring species are known to exist in nature. In addition, many of them have been broken into multiple species presumed to be evolving independently, usually obscuring the evolutionary dynamics that generate diversity. A paper in this issue of Molecular Ecology by Fuchs et al. (2015), focused on the entire genealogy of a bulbul (Alophoixus) species complex, offers key insights into the evolutionary processes underlying diversification of this Indo-Malayan bird. Their findings fulfil most of the criteria that can be expected for ring species (Fig. 1): an ancestor has colonized the mainland from Sundaland, expanded along the forested habitat wrapping around Thailand's lowlands, adjacent taxa intergrade around the ring distribution, and terminal taxa overlap at the ring closure. Although it remains unclear whether ring divergence has resulted in restrictive gene flow relative to that observed around the ring, their results suggest that circular overlaps might be more common in nature than currently recognized in the literature. Most importantly, this work shows that the continuum of species formation that Mayr and Dobzhansky praised in circular overlaps is found in biological systems currently described as 'rings of species', in addition to the idealized 'ring species'.

Phylogeography reveals an ancient cryptic radiation in East-Asian tree frogs (Hyla japonica group) and complex relationships between continental and island lineages

“…As recently emphasized, ring-like phylogeographic patterns might be more common than previously assumed [55, 56], especially in regions with complex topography and Pleistocene climatic instability [57]. Ancestral ring diversifications can sometimes also be later “broken into multiple species presumed to be evolving independently, usually obscuring the evolutionary dynamics that generate diversity” [58, 59], a scenario that would be in line with the split and seemingly independent history of our two separate taxa n. t. A and B around the Sea of Japan. Future population genetic studies might help to determine the role of isolation-by-distance in shaping H. japonica ’s diversity around the Sea of Japan and test whether the northern, terminal mtDNA lineages A1 (n. t. A) and B5 (n. t. B) interact and “close” this ring (i.e.…”

Phylogeography and population genetics reveal ring species patterns in a highly polymorphic California lily

“…One model that reconciles local adaptation in the face of gene flow is a ring species complex. Ring species provide an opportunity to explore the evolution of geographically distributed traits through the generation and maintenance of morphological gradation across genetically interconnected subpopulations (Pereira & Wake, 2015). Under a ring species model, subpopulations are expected to have accumulated mutations, and experience genetic drift and local adaptation, with differences often but not necessarily manifested into different phenotypes (Kuchta & Wake, 2016).…”

Ring distribution patterns—diversification or speciation? Comparative phylogeography of two small mammals in the mountains surrounding the Sichuan Basin

“…In fact, even in classic ring species cases, it is difficult to find strict reproductive isolation (Kuchta & Wake, 2016). Because gene flow resumes again after secondary contact (Alcaide et al, 2014;Devitt et al, 2011;Pereira & Wake, 2015), and the identification of full reproductive isolation (valid species) remains difficult (Liebers et al, 2004).…”

“…In fact, even in classic ring species cases, it is difficult to find strict reproductive isolation (Kuchta & Wake, 2016). Because gene flow resumes again after secondary contact (Alcaide et al, 2014; Devitt et al, 2011; Pereira & Wake, 2015), and the identification of full reproductive isolation (valid species) remains difficult (Liebers et al, 2004). Thus, Monahan et al, (2012) used “ring diversification” to describe the situation in which populations diverge around a geographical barrier in a ring‐like manner, regardless of whether reproductive isolation occurs at the terminus, such as for the eastern tree frog ( Hyla orientalis ) around the Black Sea (Dufresnes et al, 2016) and the odorous frog ( Odorrana margaretae ) around the Sichuan Basin (Qiao et al, 2018).…”